Data Sheet on Dendrolimus Sibiricus and Dendrolimus Superans

EuropeanBlackwell Publishing, Ltd. and Mediterranean Plant Protection Organization Organisation Européenne et Méditerranéenne pour la Protection des Plantes

Data sheets on quarantine pests Fiches informatives sur les organismes de quarantaine

Dendrolimus sibiricus and Dendrolimus superans

Identity Hosts Taxonomic position: Insecta: Lepidoptera: Lasiocampidae D. sibiricus and D. superans can damage more than 20 species Notes on taxonomy and nomenclature: Dendrolimus of Abies, Pinus, Larix, Picea and Tsuga. They can develop on sibiricus and Dendrolimus superans are two closely related practically all coniferous species in their natural area. The allopatric taxa, the former widespread in continental Russia preferred hosts of D. sibiricus are: Abies sibirica, Abies and the latter present in Sakhalin, the Kurile Islands and nephrolepis, Pinus sibirica, Pinus koraiensis, Larix gmelinii, northern Japan. According to the main international Larix sibirica, Picea ajanensis, Picea obovata. Those of opinion, these are two separate species. However, many D. superans are: Pinus pumila, Larix kamtschatica, Picea Russian scientists consider that there is a single species D. ajanensis and Abies sachalinensis (Rozhkov, 1963; Epova, superans with two subspecies: Dendrolimus superans sibiricus Pleshanov, 1995). There are no speciﬁc reports concerning Tschetverikov and Dendrolimus superans albolineatus Butler European species of conifers. (Rozhkov, 1963; Epova & Pleshanov, 1995). The two species are very similar and are treated together in this data Geographical distribution sheet.

Dendrolimus sibiricus Dendrolimus sibiricus EPPO region: Russia (eastern part of European Russia and Name: Dendrolimus sibiricus Chetverikov practically all Asian Russia except the extreme north, Sakhalin Synonyms: Dendrolimus superans sibiricus Chetverikov, and Kurile Islands; Fig. 1) Dendrolimus laricis Chetverikov Asia: Russia (practically all Asian Russia except the extreme Common names: Siberian silk moth, Siberian moth, Siberian north, Sakhalin and Kurile Islands), Kazakhstan, China conifer silk moth, Siberian lasiocampid, larch caterpillar (in (Heilongjiang, Jilin, Liaoning, Neimenggu), Korea Democratic China) (English); сибирский шелкопряд (Russian) People’s Republic, Korea Republic, Mongolia (north) EPPO code: DENDSI EU: absent Phytosanitary categorization: EPPO A2 action list no. D. sibiricus is presumed to have originated in Siberia but has 308 apparently been spreading westwards at a rate that has been variously estimated as 12 km per year or 40–50 km per year. In 1955, Okunev (1955) considered that it had reached longitude 37° Dendrolimus superans or 38° in European Russia (including the White Sea coast), but Name: Dendrolimus superans Butler a later opinion (Rozhkov, 1963) places the most western point Synonyms: Dendrolimus superans albolineatus Butler, much further to the east, at longitude 52° (Fig. 1). The furthest Dendrolimus albolineatus Matsumura, Dendrolimus yezoensis west at which outbreaks of D. sibiricus have occurred were in the Matsumura, Odonestis superans Butler regions of Perm and Udmurtia (Koltunov et al., 1997; Gninenko, Common names: white-lined silk moth, Sakhalin silk moth, 1999), but in 2001, males of the species were captured in Japanese hemlock caterpillar (English), feuille morte du tsuga pheromone traps more than 1000 km to the west, close to Moscow. du Japon (French), Japanischer Douglasien-Spinner (German), белополосый шелкопряд (Russian), tuga-kareha (Japanese) Dendrolimus superans EPPO code: DENDSU Phytosanitary categorization: EPPO A2 action list EPPO region: Russia (Sakhalin, Kurile Islands). no. 330 Asia: Japan (Hokkaido and northern Honshu), Russia

Dendrolimus sibiricus and Dendrolimus superans 391

Fig. 1 Geographical distribution of Dendrolimus sibiricus (Rozhkov, 1963).

(Sakhalin, Kurile Islands) (Matsumura, 1925; Rozhkov, 1963; the end of April, in the following year, the larvae return to the Epova, Pleshanov, 1995). crowns, eat complete needles, and sometimes the bark of young EU: absent shoots and cones. They moult after one month and again at the end of July or in August. In autumn, the larvae return to the soil and overwinter for a second time. In May and June of the Biology following year, the larvae feed very intensively. During this period, they eat about 95% of the food that they need for their Dendrolimus sibiricus development and it is then that the major damage occurs. In total, larvae moult 5–7 times and have, correspondingly, 6–8 The host/parasite relationship of D. sibiricus is characterized instars. In June, the larvae make cocoons and the development by cycles of slow build-up of population numbers over several of pupae within them takes about one month. The full life cycle years, reaching a peak (outbreak) followed by a population usually takes two years. In southern parts of the natural range, collapse. Outbreaks of D. sibiricus occur with a periodicity however, one generation can develop in a single year, whereas, of 10–11 years (Rozhkov, 1963; Epova & Pleshanov, 1995; in northern regions, the completion of a generation can Vorontsov, 1995), usually last 2–3 years and are often preceded sometimes take three years (Rozhkov, 1963; Galkin, 1993; by 2–3 years of water deficit. It has been noticed that the Vorontsov, 1995). cycle of these outbreaks in some parts of the geographical range of the pest coincides with the cycle of solar activity, with the maximum development of the outbreaks occurring Dendrolimus superans in years of increasing number of sunspots (Galkin, 1975, 1992). The biology of D. superans is very similar to that of D. sibiricus. The first flight of D. sibiricus in the middle latitudes of its Outbreaks have been recorded in Sakhalin since 1920, mainly natural range usually occurs in the middle of July. Immediately in larch-pine forests in the northern part of the island. In after mating, females lay eggs on the needles, mainly in the the south, the pest damages spruce-fir forests but only one lower part of the crowns. During outbreak years, eggs are laid major outbreak has been recorded. Outbreaks also occur in throughout the tree and on the surrounding ground. One egg spruce-fir forests on the Kurile islands (Epova & Pleshanov, mass may contain few or up to 200 eggs. Each female lays an 1995). average of 200–300 eggs, with a maximum of 800 (Rozhkov, Flights of D. superans begin in June/July and last till August. 1963; Vorontsov, 1995). Egg development usually takes 13– The pest prefers mature forests (more than 50 years old). The 15 days (with an occasional maximum of 20–22). First-instar life cycle may take one or two years (or even more) depending larvae eat the edges of needles and moult in 9–12 days. Second- on climate conditions; development takes much longer in the instar larvae cause even more damage to the needles and north of Sakhalin than in the south (Bushmelev & Yurchenko, develop for 3–4 weeks before moulting. Third-instar larvae 1989; Gninenko & Baranchikov, 2004), and presumably than descend to the soil in September and overwinter under moss. At in Japan.

392 Data sheets on quarantine pests

Fig. 3 Caterpillar of Dendrolimus sibiricus.

Fig. 4 Caterpillar before pupation and pupa of Dendrolimus sibiricus.

Fig. 2 Egg masses of Dendrolimus sibiricus. longitudinal stripe; each segment dorsally covered with silvery scales, reflecting a light shade of golden, so that in fresh specimens the dorsal hexagonal markings not distinct; stigma yellowish-white, on its sides with some reddish Detection and identification markings and white scales; dorsal marking of each abdominal segment hexagonal. Ventral surface with a series of Symptoms fuscous spots (D. sibiricus) or a yellowish-brown stripe Defoliation of Pinus, Larix, Abies or Picea spp. is usually very (D. superans) (Matsumura, 1925; Bushmelev & Yurchenko, spectacular. The presence of caterpillars is easily detected. The 1989). caterpillars and adults can easily be distinguished from related species, even from the European Dendrolimus pini, which is the Pupa most closely related species. Adult males can be captured using The pupa (Fig. 4) is brown, 33–39 mm long in females, 28– pheromone traps containing a specific pheromone (Pletniev 34 mm in males. et al., 1999). Adult The female wingspan is 60–80 mm in D. sibiricus (Fig. 5) and Morphology 77–102 mm in D. superans, and the male 40–60 or 60–79 mm, Eggs respectively. The female body length averages 39 mm, and the About 2.2 × 1.9 mm, elongate, light-green when laid, turning male 31 mm, in D. sibiricus. The following description applies creamy-white, then becoming darker and spotted (Fig. 2). to both species: colour from light yellowish-brown or light grey to dark brown or almost black; fore wings crossed by two Larva characteristic dark stripes; white spot situated at the centre of The caterpillar (Fig. 3) is 50–80 (D. sibiricus) or 60–82 the fore wing; antemedial line to the primaries straight from the (D. superans) mm long. The following description of the full- costa to the discoidal spot, then becoming oblique, reaches grown caterpillar applies to both species: mainly black or the hind margin at the inner side of the discoidal spot; vein 9 to dark-brown with numerous spots, with long hairs; the 2nd the primaries opening at the costa and not reaching apex. The and 3rd segments crossed by blue-black stripes; labrum in the postmedial line is much incurved near the costa in D. sibiricus middle shallowly incised, epicranium fuscous maculated, in and only slightly incurved in D. superans (Matsumura, 1925; the middle with a pale on each side with a yellowish-brown Bushmelev & Yurchenko, 1989).

Dendrolimus sibiricus and Dendrolimus superans 393

guttulata (Pavlovskii & Shtakelberg, 1955; Rozhkov, 1963; Mamaev, 1990; Epova & Pleshanov, 1995; Vorontsov, 1995). These pests are able to kill trees which are heavily stressed by D. sibiricus. Forests may also be predisposed to forest ﬁres. Reforestation of affected areas is often very complicated and takes much time, resulting in serious changes in the environment over large areas.

Dendrolimus superans D. superans is similar in importance on Sakhalin. In 1959/1964, the pest severely damaged larch-pine forests on 15 356 ha, and caused the death of 6526 ha of forests (Govorukhin, 1965). In 1986/1989, the pest caused the death of 1800 ha of forests (Pechenina, 1991). During outbreaks, pest populations reach 300–1000 pupae per tree, trees can be defoliated during 2–3 successive years and many trees are unable to withstand such Fig. 5 Cocoon and neonate adult moth of Dendrolimus sibiricus. a long period of defoliation. Dry forests situated on slopes of southern and south-western exposure are most susceptible. Furthermore, as for D. sibiricus, outbreaks of D. superans are very often followed by outbreaks of wood borers (scolytids, Pathways for movement cerambycids and others). These pests are able to kill trees Both species can spread by ﬂight of the adult moths (up to which are heavily stressed by D. superans (Govorukhin, 1965; 100 km per year) (Rozhkov, 1963). All stages of the life cycle Bushmelev & Yurchenko, 1989; Pechenina, 1991; Gninenko & can be transported on plants moving in trade, particularly plants Baranchikov, 2004). Similar outbreaks of D. superans occur in for planting and cut branches (including Christmas trees). northern Japan (Maeto, 1991). It may be noted that other During outbreaks especially, eggs and larvae may be associated Dendrolimus spp., e.g. Dendrolimus spectabilis (Butler), occur with wood carrying bark, or isolated bark, and may be present further south in Japan, and in Korea, and probably present as contaminating pests on other products. a similar risk, although they have not been evaluated in detail.

Pest significance Control Significant control efforts against D. sibiricus and D. superans Economic impact (mainly aerial treatment with chemical and bacterial products) Dendrolimus sibiricus are undertaken during outbreak years in Russia (Ivliev, 1960; D. sibiricus is the most important defoliator of coniferous trees Ageenko, 1969; Baranovskii, Remorov & Lamikhov, 1988; (Pinus sibirica, Larix sibirica, Abies sibirica, Picea obovata) in Maslov, 1988; Bushmelev & Yurchenko, 1989; Epova & Russia and Kazakhstan (Rozhkov, 1963; Epova & Pleshanov, Pleshanov, 1995; Vorontsov, 1995) and other countries within 1995; Vorontsov, 1995), and one of the most important the range of the pests. defoliators of Larix gmelinii in China (Yang & Gu, 1995). Under non-outbreak conditions, the natural enemies of Outbreaks occur over enormous areas (many thousands of D. sibiricus (the egg parasitoids Telenomus gracilis, Telenomus hectares) and often lead to the death of entire forests. The tetratomus, Trichogramma dendrolimi, Ooencyrtus pinicolus; evaluation made by Florov (1948) showed that, during a period the larval and pupal parasitoid Rhogas dendrolimi; the micro- of 90 years (1855–1945), D. sibiricus killed at least 4 million organisms Bacillus dendrolimus, Bacillus thuringiensis, Beau- ha of Russian forests. According to Kolomets (1958), during veria bassiana, polyhedrosis viruses and some other viruses) the 25-year period 1932–1957, D. sibiricus damaged 7 million play an important role in the regulation of its population density ha of forests in Western Siberia and Chita Oblast alone, causing (Nikiforov, 1970; Gorshkov, 1973; Baranovskii, Remorov & the death of forests in half of this area. Similar data has been Lamikhov, 1988; Yang & Gu, 1995; Vorontsov, 1995). An even published by many other scientists (e.g. Rozhkov, 1963). longer list, additional to the above, is available for D. superans: During outbreaks, trees can be defoliated during 2–3 succes- Telenomus dendrolimusi, Pachyneuron solitarius, Exorista lar- sive years and many trees are unable to withstand such a long varum, Masicera ashingivora, M. zimini, Apanteles ordinarius, period of defoliation. Furthermore, the outbreaks of D. sibiricus Apanteles liparidis, Campoplex leptogaster, Stylocryptor are also very often followed by outbreaks of wood borers profligator, Anilasta valida, Habronyx heros, Exochilum (scolytids, cerambycids and others), particularly Ips typographus, giganteum, Isorepus stercorator, Agria punctata, Echynomia Ips subelongatus (OEPP/EPPO, 2005a), Scolytus morawitzi magna, Larvaevora larvarum, Pimpla instigator, Pimpla dis- (OEPP/EPPO, 2005b), Monochamus galloprovincialis, paris, Pimpla pluto, Pimpla tabatai, Apechtis dendrolimi, Xylotrechus altaicus (OEPP/EPPO, 2005c), Melanophila Parasarcophaga uliginisa, Parasarcophaga albiceps,

Pseudosarcophaga affinis and Sarcophaga carnaria; many Epova VI & Pleshanov AS (1995) [Forest Regions Injured by Leaf-eating species of coleopteran (mainly Carabidae), hemipteran (mainly insects in Asian Russia.] Nauka, Novosibirsk (RU) (in Russian). Pentatomidae and Reduviidae) and hymenopteran predators. Florov DN (1948) [A Pest of Siberian Forests (Dendrolimus sibiricus).] OGIZ, Irkutsk (RU) (in Russian). The most numerous and efficient natural enemies of D. superans Galkin GI (1975) [Outbreaks of Dendrolimus sibiricus and solar activity.] seems to be Telenomus spp., which usually infests 20–40% Lesnoe Khozyaistvo no. 8, 83–85 (in Russian). of eggs of the pest. During outbreaks, the parasitization level Galkin GI (1992) [Periodicity of mass multiplication of pests.] Zashchita may reach 35% of larvae and 70% of pupae (Matsumura, 1925; Rastenii no. 12, 37–39 (in Russian). Ivliev, 1960; Kasparyan, 1965; Bushmelev & Yurchenko, Galkin GI (1993) [Biology of Dendrolimus superans sibiricus in Evenkia.] 1989; Yurchenko & Turova, 2002; Gninenko & Baranchikov, Zoologicheskii Zhurnal 72, 142–146 (in Russian). 2004). Gninenko YuI (1999) [Problems of forest protection against Dendrolimus sibiricus.] In: [Protection of Taiga Forests of Siberia against Dendrolimus sibiricus] (Eds Gninenko YuI, Liamtsev NI & Ferbikov VA). Proceedings Phytosanitary risk of Scientific-Practical Seminar, Gorno-Altaisk, pp. 12–18 (in Russian). Gninenko YuI & Baranchikov YuN (2004) [Dendrolimus superans yezoensis.] D. sibiricus and D. superans are both considered as very serious In: Sakhalin Coniferous Forests (in Russian) (in press). defoliators of coniferous forests in the areas where they occur Gorshkov NV (1973) [Role of egg parasites in regulating the population and are very likely to be able to establish in most EPPO of Dendrolimus sibiricus.] Lesnoe Khozyaistvo no. 4, 75–77 (in Russian). countries, particularly those in the north and centre of the Govorukhin VI (1965) [Report of forest-pathological survey of Okhta region. It is very likely that these Dendrolimus spp., which have leskhoz of the Sakhalinles enterprise of the Far East Sovnarkhoz.] Izdatel’stvo a wide host range on different conifer genera in their native 5-oi Moskovskoi AFLU Ekspeditsii V/O Lesproekt, Moscow (RU) (in range, should be able to attack other species of the same genera Russian). in the western part of the EPPO region, where they are Ivliev LA (1960) [Parasites of Dendrolimus superans in the Far East and neigh- important forest and amenity trees. bouring countries.] Soobshcheniya Dal’nevostochnogo Filiala Sibirskogo Otdeleniya Akademii Nauk SSSR no. 12, 119–153 (in Russian). Kasparyan DR (1965) [Parasites of Dendrolimus superans albolineatus in Phytosanitary measures the north of Sakhalin.] Trudy Dal’nevostochnogo Nauchno Issledova- tel’skogo Instituta Lesnogo Khozyaistva no. 7, 520–526 (in Russian). D. sibiricus was added in 2002 to the EPPO A2 action list, and Kolomets NG (1958) [Phytocenological characteristics of outbreaks of Sibe- endangered EPPO member countries are thus recommended rian silk moth in Western Siberia.] First Inter-Universities Conference on to regulate it as a quarantine pest. Similarly, D. superans was Forest Protection, pp. 37–38. Moscow (RU) (in Russian). added to the list in 2005. D. sibiricus is apparently slowly Koltunov EV, Fedorenko SI & Okhlupin OV (1997) [Dendrolimus sibiricus spreading westwards, and it may be useful, in areas at the in the spruce-fir forests of the plains east of the Urals.] Lesnoe Khozyaistvo no. 2, 51–52 (in Russian). border of the present range, for surveys to be conducted using Maeto K (1991) Outbreaks of Dendrolimus superans related to weather in pheromone traps (Pletniev et al., 1999) to detect entry of the Hokkaido. Applied Entomology and Zoology 26, 275–277. pest, and for control measures to be used for suppression of the Mamaev YB (1990) [Outbreaks of stem pests in larch forests of the Tuva pest, with a view to containment and eradication. D. superans ASSR damaged by Dendrolimus sibiricus.] Izvestiya Vysshikh Ucheb- is relatively unlikely to invade the adjoining areas where nykh Zavedenii – Lesnoi Zhurnal no. 2, 16–19 (in Russian). D. sibiricus already occurs, and so presents more of an A1 risk Maslov AD (1988) [Guide to Forest Protection against Pests and Diseases.] Agropromizdat, Moscow (RU) (in Russian). to the western part of the EPPO region. Matsumura S (1925) On the three species of Dendrolimus which attack To prevent introduction of both D. sibiricus and D. superans spruce and fir trees in Japan, with their parasites and predaceous insects. by international movement of commodities, plants for planting Annals of the Zoological Institute of the Academy of Sciences of the USSR and cut branches of host plants from the infested areas should XXVI, 27–50. be free from soil according to OEPP/EPPO (1994). Alterna- Nikiforov GM (1970) [The characteristics of a massive outbreak of Den- tively, such commodities could originate in a pest-free area, be drolimus sibiricus.] Zashchita Rastenii no. 9, 38–39 (in Russian). produced in protected houses, or fumigated, or imported during OEPP/EPPO (1994) EPPO Standard PM 3/54 Growing plants in growing medium prior to export. Bulletin OEPP/EPPO Bulletin 24, 326–327. winter. Wood should be debarked or heat-treated, or originate in Okunev PP (1955) [Geographical distribution and zones of injuriousness of a pest-free area, or be imported during winter, and isolated bark Dendrolimus Sibiricus.] In: [Geographical Problems in Forestry], Vol. 5, should be treated to destroy contaminating insects. pp. 32–48. Izdatel’stvo Akademii Nauk SSSR, Moscow–Leningrad (RU) (in Russian). Pavlovskii EN & Shtakelberg AA (1955) [Guide to Forest Pests.] Izdatel’stvo References Akademii Nauk SSSR, Moscow–Leningrad (RU) (in Russian). Ageenko AS, ed. (1969) [Forests of the Far East.] Lesnaya Promyshlennost, Pechenina TV (1991) [Report of forest-pathological survey of Anivsk, Moscow (RU) (in Russian). Dolinsk, Korsakov, Krasnogorsk, Okhta, Smirnykhovsk, Tomari, Kholmsk, Baranovskii VI, Remorov VV & Lamikhov KL (1988) [Ecological aspects Yuzhno-Sakhalinsk leskhozes of Sakhalin forestry association.] Izdatel’stvo of the use of micro-organisms against Dendrolimus sibiricus.] Lesnoe Moskovskogo Spetsializirovannogo Lesoustroitel’nogo Predpriyatiya, Khozyaistvo no. 8, 54–55 (in Russian). Moscow (RU) (in Russian). Bushmelev IV & Yurchenko GI (1989) [Study of Dendrolimus superans Pletniev VA, Vendiilo NV, Ponomarev VL, Mitroshin DB & Lebed’eva KB albolineatus on Sakhalin.] Trudy Dal’nevostochnogo Nauchno Issledova- (1999) [The search for a pheromone of Dendrolimus sibiricus.] In: tel’skogo Instituta Lesnogo Khozyaistva no. 31, 119–125 (in Russian). [Protection of Taiga Forests of Siberia against Dendrolimus sibiricus]

(Eds Gninenko YI, Liamtsev NI & Ferbikov VA), pp. 56–57. Gorno- Yang ZQ & Gu YQ (1995) [Egg-parasitic wasps of the larch caterpillar in Altaisk (RU) (in Russian). Daxing-anling mountains with description of new species.] Scientia Rozhkov AS (1963) [Dendrolimus sibiricus.] Izdatel’stvo Akademii Nauk Silvae Sinicae 31, 223–231 (in Chinese). SSSR, Moscow (RU) (in Russian). Yurchenko GI & Turova GI (2002) [Parasites of Dendrolimus sibiricus and Vorontsov AI (1995) [Forest Entomology.], 5th edn. Ekologiya, Moscow D. superans in the Far East of Russia.] Entomologicheskie Issledovaniya (RU) (in Russian). v Sibiri no. 2, 75–86 (in Russian).